The progression of replication forks at natural replication barriers in live bacteria

Nucleic Acids Research

Volumn 44, Issue 13, 2016, Pages 6262-6273

  Moolman, M Charl ^a   Tiruvadi Krishnan, Sriram ^a   Kerssemakers, Jacob W J ^a   De Leeuw, Roy ^a   Lorent, Vincent ^b   Sherratt, David J ^c   Dekker, Nynke H ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b UNIVERSITÉ PARIS 13   (France)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; TUS PROTEIN; UNCLASSIFIED DRUG; DNA HELICASE; DNA REPLICATION TERMINUS SITE-BINDING PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; MACROMOLECULE; TUS PROTEIN, E COLI;

ARTICLE; CHROMOSOME SEGREGATION; DNA PROTEIN COMPLEX; DNA REPLICATION; DNA SEQUENCE; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; MICROFLUIDICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; REPLISOME; BACTERIAL CHROMOSOME; GENETICS; MACROMOLECULE; METABOLISM;

CHROMOSOME SEGREGATION; CHROMOSOMES, BACTERIAL; DNA HELICASES; DNA REPLICATION; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MACROMOLECULAR SUBSTANCES;

EID: 84982074338     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw397     Document Type: Article

References (66)

1. Johnson, A. and O'Donnell, M. (2005) Cellular DNA replicases: components and dynamics at the replication fork. Annu. Rev. Biochem., 74, 283-315.
2. McHenry, C.S. (2011) DNA replicases from a bacterial perspective. Annu. Rev. Biochem., 80, 403-436.
3. Duderstadt, K.E., Reyes-Lamothe, R., van Oijen, A.M. and Sherratt, D.J. (2013) Replication-Fork Dynamics. Cold Spring Harb. Perspect. Biol., 6, 1-17.
4. Reyes-Lamothe, R., Possoz, C., Danilova, O. and Sherratt, D.J. (2008) Independent positioning and action of Escherichia coli replisomes in live cells. Cell, 133, 90-102.
5. Jun, S. and Wright, A. (2010) Entropy as the driver of chromosome segregation. Nat. Rev. Microbiol., 8, 600-607.
6. Kuwada, N.J., Cheveralls, K.C., Traxler, B. and Wiggins, P.A. (2013) Mapping the driving forces of chromosome structure and segregation in Escherichia coli. Nucleic Acids Res., 41, 7370-7377.
7. Di Ventura, B., Knecht, B., Andreas, H., Godinez, W.J., Fritsche, M., Rohr, K., Nickel, W., Heermann, D.W. and Sourjik, V. (2013) Chromosome segregation by the Escherichia coli Min system. Mol. Syst. Biol., 9, 686.
8. Fisher, J.K., Bourniquel, A., Witz, G., Weiner, B., Prentiss, M. and Kleckner, N. (2013) Four-dimensional imaging of E. coli nucleoid organization and dynamics in living cells. Cell, 153, 882-895.
9. Youngren, B., Nielsen, H.J., Jun, S. and Austin, S. (2014) The multifork Escherichia coli chromosome is a self-duplicating and self-segregating thermodynamic ring polymer. Genes Dev., 28, 71-84.
10. Merrikh, H., Zhang, Y., Grossman, A.D. and Wang, J.D. (2012) Replication-transcription conflicts in bacteria. Nat. Rev. Microbiol., 10, 449-458.
11. Michel, B., Grompone, G., Florès, M.-J. and Bidnenko, V. (2004) Multiple pathways process stalled replication forks. Proc. Natl. Acad. Sci. U.S.A., 101, 12783-12788.
12. Gupta, M.K., Guy, C.P., Yeeles, J.T.P., Atkinson, J., Bell, H., Lloyd, R.G., Marians, K.J. and McGlynn, P. (2013) Protein-DNA complexes are the primary sources of replication fork pausing in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A., 110, 7252-7257.
13. Hill, T.M., Tecklenburg, M.L., Pelletier, A.J. and Kuempel, P.L. (1989) tus, the trans-acting gene required for termination of DNA replication in Escherichia coli, encodes a DNA-binding protein. Proc. Natl. Acad. Sci. U.S.A., 86, 1593-1597.
14. Hidaka, M., Kobayashi, T., Takenaka, S., Takeya, H. and Horiuchi, T. (1989) Purification of a DNA replication terminus (ter) site-binding protein in Escherichia coli and identification of the structural gene. J. Biol. Chem., 264, 21031-21037.
15. Hill, T.M. (1992) Arrest of bacterial DNA replication. Annu. Rev. Microbiol., 46, 603-633.
16. Coskun-Ari, F.F., Skokotas, A., Moe, G.R. and Hill, T.M. (1994) Biophysical characteristics of Tus, the replication arrest protein of Escherichia coli. J. Biol. Chem., 269, 4027-4034.
17. Rudolph, C.J., Upton, A.L., Briggs, G.S. and Lloyd, R.G. (2010) Is RecG a general guardian of the bacterial genomě DNA Repair, 9, 210-223.
18. Hill, T.M. and Marians, K.J. (1990) Escherichia coli Tus protein acts to arrest the progression of DNA replication forks in vitro. Proc. Natl. Acad. Sci. U.S.A., 87, 2481-2485.
19. Bidnenko, V., Ehrlich, S.D. and Michel, B. (2002) Replication fork collapse at replication terminator sequences. EMBO J., 21, 3898-3907.
20. Neylon, C., Kralicek, A.V., HILL, T.M. and Dixon, N.E. (2005) Replication termination in Escherichia coli: structure and antihelicase activity of the Tus-Ter complex. Microbiol. Mol. Biol. Rev., 69, 501-526.
21. Duggin, I.G., Wake, R.G., Bell, S.D. and Hill, T.M. (2008) The replication fork trap and termination of chromosome replication. Mol. Microbiol., 70, 1323-1333.
22. Kaplan, D.L. and Bastia, D. (2009) Mechanisms of polar arrest of a replication fork. Mol. Microbiol., 72, 279-285.
23. Mulcair, M.D., Schaeffer, P.M., Oakley, A.J., Cross, H.F., Neylon, C., Hill, T.M. and Dixon, N.E. (2006) A molecular mousetrap determines polarity of termination of DNA replication in E. coli. Cell, 125, 1309-1319.
24. Bastia, D., Zzaman, S., Krings, G., Saxena, M., Peng, X. and Greenberg, M.M. (2008) Replication termination mechanism as revealed by Tus-mediated polar arrest of a sliding helicase. Proc. Natl. Acad. Sci. U.S.A., 105, 12831-12836.
25. Berghuis, B.A., Dulin, D., Yu, Z., van Laar, T., Cross, B., Janissen, R., Jergic, S., Dixon, N.E., Depken, S. and Dekker, N.H. (2015) Strand separation suffices to establish a long-lived, foolproof DNA-protein lock at the Tus-Ter replication fork barrier. Nat. Chem. Biol., 11, 579-585.
26. Gottlieb, P.A., WU, S., Zhang, X., Tecklenburg, M., Kuempel, P. and Hill, T.M. (1992) Equilibrium, kinetic, and footprinting studies of the Tus-Ter protein-DNA interaction. J. Biol. Chem., 267, 7434-7443.
27. Neylon, C., Brown, S.E., Kralicek, A.V., Miles, C.S., Love, C.A. and Dixon, N.E. (2000) Interaction of the Escherichia coli replication terminator protein (Tus) with DNA: a model derived from DNA-binding studies of mutant proteins by surface plasmon resonance. Biochemistry, 39, 11989-11999.
28. Lewis, P.J., Ralston, G.B., Christopherson, R.I. and Wake, R.G. (1990) Identification of the replication terminator protein binding sites in the terminus region of the Bacillus subtilis chromosome and stoichiometry of the binding. J. Mol. Biol., 214, 73-84.
29. Bussiere, D.E., Bastia, D. and White, S.W. (1995) Crystal structure of the replication terminator protein from B. subtilis at 2.6 A. Cell, 80, 651-660.
30. Lemon, K.P., Kurtser, I. and Grossman, A.D. (2001) Effects of replication termination mutants on chromosome partitioning in Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A., 98, 212-217.
31. Willis, N.A., Chandramouly, G., Huang, B., Kwok, A., Follonier, C., Deng, C. and Scully, R. (2014) BRCA1 controls homologous recombination at Tus/Ter-stalled mammalian replication forks. Nature, 510, 556-559.
32. Larsen, N.B., Sass, E., Suski, C., Mankouri, H.W. and Hickson, I.D. (2014) The Escherichia coli Tus-Ter replication fork barrier causes site-specific DNA replication perturbation in yeast. Nat. Commun., 5, 3574.
33. Hill, T.M., Henson, J.M. and Kuempel, P.L. (1987) The terminus region of the Escherichia coli chromosome contains two separate loci that exhibit polar inhibition of replication. PNAS, 84, 1754-1758.
34. Duggin, I.G. and Bell, S.D. (2009) Termination structures in the Escherichia coli chromosome replication fork trap. J. Mol. Biol., 387, 532-539.
35. Moreau, M. J.J. and Schaeffer, P.M. (2012) Differential Tus-Ter binding and lock formation: implications for DNA replication termination in Escherichia coli. Mol. Biosyst., 8, 2783-2791.
36. Pomerantz, R.T. and O'Donnell, M. (2010) Direct restart of a replication fork stalled by a head-on RNA polymerase. Science, 327, 590-592.
37. Yeeles, J.T.P. and Marians, K.J. (2011) The Escherichia coli replisome is inherently DNA damage tolerant. Science, 334, 235-238.
38. Wang, X., Lesterlin, C., Reyes-Lamothe, R., Ball, G. and Sherratt, D.J. (2011) Replication and segregation of an Escherichia coli chromosome with two replication origins. Proc. Natl. Acad. Sci. U.S.A., 108, E243-E250.
39. Ivanova, D., Taylor, T., Smith, S.L., Dimude, J.U., Upton, A.L., Mehrjouy, M.M., Skovgaard, O., Sherratt, D.J., Retkute, R. and Rudolph, C.J. (2015) Shaping the landscape of the Escherichia coli chromosome: replication-transcription encounters in cells with an ectopic replication origin. Nucleic Acids Res., 43, 7865-7877.
40. Moolman, M.C., Huang, Z., Krishnan, S.T., Kerssemakers, J.W.J. and Dekker, N.H. (2013) Electron beam fabrication of a microfluidic device for studying submicron-scale bacteria. J. Nanobiotechnol., 11, 12.
41. Rocha, E. (2004) The replication-related organization of bacterial genomes. Microbiology, 150, 1609-1627.
42. Liu, X., Wang, X., Reyes-Lamothe, R. and Sherratt, D.J. (2010) Replication-directed sister chromosome alignment in Escherichia coli. Mol. Microbiol., 75, 1090-1097.
43. Moolman, M.C., Krishnan, S.T., Kerssemakers, J.W.J., van den Berg, A., Tulinski, P., Depken, M., Reyes-Lamothe, R., Sherratt, D.J. and Dekker, N.H. (2014) Slow unloading leads to DNA-bound 2-sliding clamp accumulation in live Escherichia coli cells. Nat. Commun., 5, 5820.
44. Wang, X., Reyes-Lamothe, R. and Sherratt, D.J. (2008) Visualizing genetic loci and molecular machines in living bacteria. Biochem. Soc. Trans., 36, 749-753.
45. Possoz, C., Filipe, S.R., Grainge, I. and Sherratt, D.J. (2006) Tracking of controlled Escherichia coli replication fork stalling and restart at repressor-bound DNA in vivo. EMBO J., 25, 2596-2604.
46. Wang, X., Possoz, C. and Sherratt, D.J. (2005) Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. Genes Dev., 19, 2367-2377.
47. Wang, X., Liu, X., Possoz, C. and Sherratt, D.J. (2006) The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev., 20, 1727-1731.
48. Morigen Odsbu, I. and Skarstad, K. (2009) Growth rate dependent numbers of SeqA structures organize the multiple replication forks in rapidly growing Escherichia coli. Genes Cells, 14, 643-657.
49. Roecklein, B., Pelletier, A. and Kuempel, P. (1991) The tus gene of Escherichia coli: autoregulation, analysis of flanking sequences and identification of a complementary system in Salmonella typhimurium. Res. Microbiol., 142, 169-175.
50. Wang, X., Reyes-Lamothe, R. and Sherratt, D.J. (2008) Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev., 22, 2426-2433.
51. Joshi, M.C., Bourniquel, A., Fisher, J., Ho, B.T., Magnan, D., Kleckner, N. and Bates, D. (2011) Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps. Proc. Natl. Acad. Sci. U.S.A., 108, 2765-2770.
52. Nielsen, H.J., Youngren, B., Hansen, F.G. and Austin, S. (2007) Dynamics of Escherichia coli chromosome segregation during multifork replication. J. Bacteriol., 189, 8660-8666.
53. Wang, X., Montero Llopis, P. and Rudner, D.Z. (2013) Organization and segregation of bacterial chromosomes. Nat. Rev. Genet., 14, 191-203.
54. Mettrick, K.A. and Grainge, I. (2015) Stability of blocked replication forks in vivo. Nucleic Acids Res., 44, 657-668.
55. Mercier, R., Petit, M.A., Schbath, S., Robin, S. and El Karoui, M. (2008) The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell, 135, 475-485.
56. Rudolph, C.J., Upton, A.L., Stockum, A., Nieduszynski, C.A. and Lloyd, R.G. (2013) Avoiding chromosome pathology when replication forks collide. Nature, 500, 608-611.
57. Hendrickson, H. and Lawrence, J.G. (2007) Mutational bias suggests that replication termination occurs near the dif site, not at Ter sites. Mol. Microbiol., 64, 42-56.
58. Lesterlin, C., Barre, F.-X. and Cornet, F. (2004) Genetic recombination and the cell cycle: what we have learned from chromosome dimers. Mol. Microbiol., 54, 1151-1160.
59. Georgescu, R.E., Yao, Y.N. and O'Donnell, M. (2010) Single-molecule analysis of the Escherichia coli replisome and use of clamps to bypass replication barriers. FEBS Lett., 584, 2596-2605.
60. Shereda, R.D., Kozlov, A.G. and Lohman, T.M. (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol., 43, 289-318.
61. Boubakri, H., de Septenville, A.L., Viguera, E. and Michel, B. (2010) The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. EMBO J., 29, 145-157.
62. Hiasa, H. and Marians, K.J. (1992) Differential inhibition of the DNA translocation and DNA unwinding activities of DNA helicases by the Escherichia coli Tus protein. J. Biol. Chem., 267, 11379-11385.
63. Sherratt, D.J., Arciszewska, L.K. and Crozat, E. (2010) The Escherichia coli DNA translocase FtsK. Biochem. Soc., 38, 395-398.
64. Grainge, I. (2013) Simple topology: FtsK-directed recombination at the dif site. Biochem. Soc. Trans., 41, 595-600.
65. Lee, J.Y., Finkelstein, I.J., Arciszewska, L.K., Sherratt, D.J. and Greene, E.C. (2014) Single-molecule imaging of FtsK translocation reveals mechanistic features of protein-protein collisions on DNA. Mol. Cell, 54, 832-843.
66. Kamada, K., Horiuchi, T., Ohsumi, K., Shimamoto, N. and Morikawa, K. (1996) Structure of a replication-terminator protein complexed with DNA. Nature, 383, 598-603.